Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses.

Phylogenetic analyses suggest that long-terminal repeat (LTR) bearing retrotransposable elements can acquire additional open-reading frames that can enable them to mediate infection. Whereas this process is best documented in the origin of the vertebrate retroviruses and their acquisition of an envelope (env) gene, similar independent events may have occurred in insects, nematodes, and plants. The origins of env-like genes are unclear, and are often masked by the antiquity of the original acquisitions and by their rapid rate of evolution. In this report, we present evidence that in three other possible transitions of LTR retrotransposons to retroviruses, an envelope-like gene was acquired from a viral source. First, the gypsy and related LTR retrotransposable elements (the insect errantiviruses) have acquired their envelope-like gene from a class of insect baculoviruses (double-stranded DNA viruses with no RNA stage). Second, the Cer retroviruses in the Caenorhabditis elegans genome acquired their envelope gene from a Phleboviral (single ambisense-stranded RNA viruses) source. Third, the Tas retroviral envelope (Ascaris lumricoides) may have been obtained from Herpesviridae (double-stranded DNA viruses, no RNA stage). These represent the only cases in which the env gene of a retrovirus has been traced back to its original source. This has implications for the evolutionary history of retroviruses as well as for the potential ability of all LTR-retrotransposable elements to become infectious agents.

[1]  C. Lloréns,et al.  Ty3/Gypsy retrotransposons: description of new Arabidopsis thaliana elements and evolutionary perspectives derived from comparative genomic data. , 2000, Molecular biology and evolution.

[2]  A. Lewin,et al.  Systematic screening of Anopheles mosquito genomes yields evidence for a major clade of Pao‐like retrotransposons , 2000, Insect molecular biology.

[3]  Shmuel Pietrokovski,et al.  Increased coverage of protein families with the Blocks Database servers , 2000, Nucleic Acids Res..

[4]  Alejandro A. Schäffer,et al.  IMPALA: matching a protein sequence against a collection of PSI-BLAST-constructed position-specific score matrices , 1999, Bioinform..

[5]  J. Vlak,et al.  Sequence and organization of the Spodoptera exigua multicapsid nucleopolyhedrovirus genome. , 1999, The Journal of general virology.

[6]  I. K. Jordan,et al.  Evidence for the recent horizontal transfer of long terminal repeat retrotransposon. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[7]  N. Bowen,et al.  Genomic analysis of Caenorhabditis elegans reveals ancient families of retroviral-like elements. , 1999, Genome research.

[8]  K. Okano,et al.  Sequence analysis of the Xestia c-nigrum granulovirus genome. , 1999, Virology.

[9]  P. Capy,et al.  Retrotransposons and retroviruses: analysis of the envelope gene. , 1999, Molecular biology and evolution.

[10]  M. Labrador,et al.  The retrotransposon Osvaldo from Drosophila buzzatii displays all structural features of a functional retrovirus. , 1999, Molecular biology and evolution.

[11]  T. Eickbush,et al.  Modular Evolution of the Integrase Domain in the Ty3/Gypsy Class of LTR Retrotransposons , 1999, Journal of Virology.

[12]  G. Blissard,et al.  Requirement for GP64 to drive efficient budding of Autographa californica multicapsid nucleopolyhedrovirus. , 1999, Virology.

[13]  C. Funk,et al.  Sequence and analysis of the genome of a baculovirus pathogenic for Lymantria dispar. , 1999, Virology.

[14]  B. Dastugue,et al.  Mobilization of two retroelements, ZAM and Idefix, in a novel unstable line of Drosophila melanogaster. , 1999, Molecular biology and evolution.

[15]  E. Gaucher,et al.  SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  D. Voytas,et al.  Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. , 1998, Genetics.

[17]  O. Jarrett Retroviruses , 1998, Nature Medicine.

[18]  Michael Gribskov,et al.  Combining evidence using p-values: application to sequence homology searches , 1998, Bioinform..

[19]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[20]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[21]  H. Robertson,et al.  Multiple Mariner transposons in flatworms and hydras are related to those of insects. , 1997, The Journal of heredity.

[22]  S. Brunak,et al.  SHORT COMMUNICATION Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites , 1997 .

[23]  W. Britt,et al.  Human cytomegalovirus glycoproteins. , 1996, Intervirology.

[24]  S. Henikoff,et al.  Automated construction and graphical presentation of protein blocks from unaligned sequences. , 1995, Gene.

[25]  F. Müller,et al.  Tas, a retrotransposon from the parasitic nematode Ascaris lumbricoides. , 1994, Gene.

[26]  J. Boeke,et al.  An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. , 1994, Genes & development.

[27]  A. Haenni,et al.  Molecular biology of tenuiviruses, a remarkable group of plant viruses. , 1994, The Journal of general virology.

[28]  W. Maddison,et al.  Phylogenetic analysis supports horizontal transfer of P transposable elements. , 1994, Molecular biology and evolution.

[29]  B. Rost,et al.  Prediction of protein secondary structure at better than 70% accuracy. , 1993, Journal of molecular biology.

[30]  T. Eickbush,et al.  Pao, a highly divergent retrotransposable element from Bombyx mori containing long terminal repeats with tandem copies of the putative R region. , 1993, Nucleic acids research.

[31]  J. Coffin,et al.  Mechanism of transduction by retroviruses. , 1992, Science.

[32]  E. Koonin,et al.  Diverse groups of plant RNA and DNA viruses share related movement proteins that may possess chaperone-like activity. , 1991, The Journal of general virology.

[33]  T. Eickbush,et al.  Origin and evolution of retroelements based upon their reverse transcriptase sequences. , 1990, The EMBO journal.

[34]  M. Nissen,et al.  Gene organization and transcription of TED, a lepidopteran retrotransposon integrated within the baculovirus genome , 1990, Molecular and cellular biology.

[35]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[36]  H. Hanafusa,et al.  Comparison between the viral transforming gene (src) of recovered avian sarcoma virus and its cellular homolog , 1981, Molecular and cellular biology.